Alison K. Surridge

Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Evolution and selection of trichromatic vision in primates

Trichromatic colour vision is of considerable importance to primates but is absent in other eutherian mammals. Primate colour vision is traditionally believed to have evolved for finding food in the forest. Recent work has tested the ecological importance of trichromacy to primates, both by measuring the spectral and chemical properties of food eaten in the wild, and by testing the relative foraging abilities of dichromatic and trichromatic primates. Molecular studies have revealed the genetic mechanisms of the evolution of trichromacy, and are providing new insight into visual pigment gene expression and colour vision defects. By drawing together work from these different fields, we can gain a better understanding of how natural selection has shaped the evolution of trichromatic colour vision in primates and also about mechanisms of gene duplication, heterozygote advantage and balancing selection.

The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.)

SUMMARY The evolution of trichromatic colour vision by the majority of anthropoid primates has been linked to the efficient detection and selection of food, particularly ripe fruits among leaves in dappled light. Modelling of visual signals has shown that trichromats should be more efficient than dichromats at distinguishing both fruits from leaves and ripe from unripe fruits. This prediction is tested in a controlled captive setting using stimuli recreated from those actually encountered by wild tamarins (Saguinus spp.). Dietary data and reflectance spectra of Abuta fluminum fruits eaten by wild saddleback (Saguinus fuscicollis) and moustached (Saguinus mystax) tamarins and their associated leaves were collected in Peru. A. fluminum leaves, and fruits in three stages of ripeness, were reproduced and presented to captive saddleback and red-bellied tamarins (Saguinus labiatus). Trichromats were quicker to learn the task and were more efficient at selecting ripe fruits than were dichromats. This is the first time that a trichromatic foraging advantage has been demonstrated for monkeys using naturalistic stimuli with the same chromatic properties as those encountered by wild animals.

Reduced Heterozygosity Depresses Sperm Quality in Wild Rabbits, Oryctolagus cuniculus

When close relatives are forced to reproduce, the resulting offspring inherit above average homozygosity and reduced fitness. Biologists now recognize inbreeding depression in the wild, a phenomenon that will probably increase as natural populations become depleted and fragmented. Inbreeding depression is most commonly expressed as compromised fertility and embryogenesis, but actual mechanisms remain poorly understood, especially for wild populations. Here, we examine how reduced heterozygosity influences spermatozoal and gonadal traits in wild rabbits (Oryctolagus cuniculus) sampled across the United Kingdom. By using a suite of 29 microsatellite markers (analyzed to confirm representation of individual heterozygosity across our sample), we found a significant negative relationship between heterozygosity and the production of normal sperm; the relationship was significant both between (n = 12) and within (n = 91 [total males], 42 [island], 49 [mainland]) populations. Reduced heterozygosity was also associated with decreased testis size across males (n = 112), but no relationship was seen at the population level, suggesting environmental confounds. Our results show, for a wild mammal, that inbreeding is associated with decreased sperm quality, confirming suggestions of links between inbreeding and elevated sperm abnormalities in rare felids . These findings could explain why inbreeding depression so frequently arises via compromised fertility and embryogenesis .

Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates

Many New World (NW) primates possess a remarkable polymorphism in an X‐linked locus, which encodes for the visual pigments (opsins) used for colour vision. Females that are heterozygous for opsin alleles of different spectral sensitivity at this locus have trichromatic colour vision, whereas homozygous females and males are dichromatic, with poor colour discrimination in the red–green range. Here we describe an extensive survey of allelic variation in both exons and introns at this locus within and among species of the Callitrichines (marmosets and tamarins). All five genera of Callitrichines have the X‐linked polymorphism, and only the three functional allelic classes described previously (with maximum wavelength sensitivities at about 543 nm, 556 nm and 563 nm) were found among the 16 species and 233 or more X‐chromosomes sampled. In spite of the homogenizing effects of gene conversion, phylogenetic analyses provide direct evidence for trans‐specific evolution of alleles over time periods of at least 5–6 million years, and up to 14 million years (estimated from independent phylogenies). These conclusions are supported by the distribution of insertions and deletions in introns. The maintenance of polymorphism over these time periods requires an adaptive explanation, which must involve a heterozygote advantage for trichromats. The lack of detection of alleles that are recombinant for spectral sensitivity suggests that such alleles are suboptimal. The two main hypotheses for the selective advantage of trichromacy in primates are frugivory for ripe fruits and folivory for young leaves. The latter can be discounted in Callitrichines, as they are not folivorous.

Genetic evidence for hybrid trait speciation in heliconius butterflies.

Homoploid hybrid speciation is the formation of a new hybrid species without change in chromosome number. So far, there has been a lack of direct molecular evidence for hybridization generating novel traits directly involved in animal speciation. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has been proposed as a hybrid species, and its color pattern can be recreated by introgression of the H. m. melpomene red band into the genetic background of the yellow banded H. cydno cordula. This hybrid color pattern is also involved in mate choice and leads to reproductive isolation between H. heurippa and its close relatives. Here, we provide molecular evidence for adaptive introgression by sequencing genes across the Heliconius red band locus and comparing them to unlinked wing patterning genes in H. melpomene, H. cydno, and H. heurippa. 670 SNPs distributed among 29 unlinked coding genes (25,847bp) showed H. heurippa was related to H. c. cordula or the three species were intermixed. In contrast, among 344 SNPs distributed among 13 genes in the red band region (18,629bp), most showed H. heurippa related with H. c. cordula, but a block of around 6,5kb located in the 3′ of a putative kinesin gene grouped H. heurippa with H. m. melpomene, supporting the hybrid introgression hypothesis. Genealogical reconstruction showed that this introgression occurred after divergence of the parental species, perhaps around 0.43Mya. Expression of the kinesin gene is spatially restricted to the distal region of the forewing, suggesting a mechanism for pattern regulation. This gene therefore constitutes the first molecular evidence for adaptive introgression during hybrid speciation and is the first clear candidate for a Heliconius wing patterning locus.

Fine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus)

The genetic structure of a free‐living tagged population of European wild rabbits (Oryctolagus cuniculus) was investigated for two consecutive years (1990 and 1991) using 10 polymorphic microsatellite loci. A specific social behaviour, the formation of stable breeding groups, influenced the genetic structure of the population. These breeding groups were shown to constitute genetically differentiated units with low levels of gene flow between them. The average relatedness among members of a social group was higher than within the population as a whole. As a result of female philopatry coupled with male‐biased natal dispersal, the relatedness of females was higher than that of males, both within social groups and in the whole population. Furthermore, the average relatedness of females within groups was twice the relatedness of females between groups. This study reveals marked fine‐scale, intrapopulation genetic structure, which is attributable to the social behaviour of the European wild rabbit.

Evolution of the Insect Yellow Gene Family

The yellow gene family is intriguing for a number of reasons. To date, yellow-like genes have only been identified in insect species and a number of bacteria. The function of the yellows is largely unknown, although a few have been associated with melanization and behavior in Drosophila, and a unique clade of genes from Apis mellifera may be involved in caste specification. Here, we show that yellow-like sequences are present in bacteria, insects, and fungi but absent from other eukaryotes apart from isolated putative sequences in Amphioxus, the Salmon Louse, and Naegleria. The yellow-like family forms a discrete gene class characterized by the presence of a major royal jelly protein domain, but eukaryote yellow-like proteins are not monophyletic. The unusual phylogenetic distribution of yellow-like sequences suggests either multiple horizontal transfer from bacteria into eukaryotes or extensive gene loss in eukaryote lineages. Comparative analysis of yellow family synteny and gene order demonstrates that a highly conserved block of three to five genes has been maintained throughout insect diversification despite extensive genome rearrangements. We show strong purifying selection on seven yellow genes over approximately 100 My separating the silkmoth and Heliconius butterflies and an association between spatial regulation of gene expression and distribution of melanic pigment in the developing butterfly wing. A single ancestral yellow-like gene has therefore undergone multiple rounds of duplication within the insects accompanied by functional constraint on both genomic location and protein evolution.

Striped rabbits in Southeast Asia

The Annamite mountains of Laos and Vietnam have yielded several important mammalian discoveries. We have found a striped rabbit of the previously monospecific genus Nesolagus, extending its known range more than 1,500 km north from the island of Sumatra into mainland Southeast Asia. The Sumatran and mainland Annamite populations are morphologically similar, but genetic data indicate that they have been isolated for millions of years.

Dichromatic and Trichromatic Callithrix geoffroyi Differ in Relative Foraging Ability for Red-green Color-camouflaged and Non-camouflaged food

An advantage for trichromatic color vision in primates is shown by its presence in many lineages, but little attention has been paid to the potential disadvantages of trichromacy. Most New World monkey species are polymorphic for color vision, with both dichromats and trichromats present within a single population. We tested the foraging ability of trichromatic and dichromatic Geoffroys marmosets (Callithrix geoffroyi) for colored cereal balls (Kix®) under conditions of red-green color camouflage (orange/green Kix® against an orange/green background) or lack of camouflage (Kix® same color as background) in a naturalized captive setting. In separate experiments designed to test foraging ability at long distances (<6 m) and short distances (<0.5 m), trichromats found significantly fewer Kix® under the camouflage condition than in the non-camouflage condition. In contrast, there is no difference in the ability of dichromats to detect color-camouflaged versus non-camouflaged Kix®. There is no significant difference between dichromats and trichromats for either camouflaged or non-camouflaged Kix®, though the power in the tests is low because of high individual variation. The results have clear implications for the foraging strategies of trichromatic marmosets. Differences in intensity of competition between trichromats and dichromats for items of food of different colors in relation to background may also have consequences for the foraging behavior of dichromats.